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Goldenberg R, Michelangeli FA, Aona LYS, Amorim AM.2016. Angiosperms and the Linnean shortfall: three new species from three lineages of Melastomataceae at one spot at the Atlantic Forest. PeerJ4:e1824https://doi.org/10.7717/peerj.1824

Abstract

Three new species of Angiosperms have been found in four short collection trips to the same protected reserve—“Estação Ecológica Estadual de Wenceslau Guimarães”—and neighboring areas in the Atlantic Forest in the south of the Brazilian state of Bahia. These new species belong to three genera from three distinct lineages in the family Melastomataceae: Huberia, Meriania and Physeterostemon. The description of these species represent a good example of a Linnean shortfall, i.e., the absence of basic knowledge about the biodiversity in the area, as well as in tropical forests as a whole. The description of these probably endemic species per se is a signal that this area deserves more attention regarding research and policies, but its consequences go farther: this area has a relevant role as a phylogenetic (both genetic and morphological) stock, and thus is also valuable as a phylogenetic conservation priority.

Introduction

Studies on biodiversity and evolutionary biology have been traditionally hindered by gaps in basic, natural history knowledge, no matter what kind of methods or organisms they deal with. These “shortfalls” can be linked to the lack of taxonomic work, i.e., species descriptions (“Linnean shortfall”; Brown & Lomolino, 1998; Whittaker et al., 2005) or absence of data regarding their distribution (“Wallacean shortfall”; Bini et al., 2006). Both lead to a third gap in our knowledge: the lack of information on phylogenetic relationships, and thus the evolutionary history of life on Earth (i.e., “Darwinian shortfall”, Diniz-Filho et al., 2013).

The forests of eastern Brazil (Atlantic Forest or “Mata Atlântica”) harbor an incredible amount of biodiversity, and are considered one of the biodiversity hotspots (Myers et al., 2000). With less than 10% of the original vegetation remaining, the Atlantic Forest is also a high conservation priority (Myers et al., 2000; Ribeiro et al., 2009). Our knowledge about biodiversity in this area is not static as inventories of angiosperms have shown. In 2009 the list of flowering plants from the Atlantic Forest contained ca. 13,700 species (Stehmann et al., 2009), while the most recent account (BFG, 2015) includes ca. 15,000 species. In both cases 49–49.5% of the species are reported as endemic. This 1,300 species increase within six years is mainly due to the participation of specialists for most plant families and the heavy use of new informatic tools (BFG, 2015). However, this increase also includes new species being described at a steady rate. In a 16 year span (1990–2006), 1,194 species of angiosperms were described for the Atlantic Forest (Sobral & Stehmann, 2009), which represents an increase of about 80 species per year. Taking the total 13,700 species surveyed in 2009, this means that almost 8.7% of these species were described in the previous 15 years.

The discovery of three distantly related species in the same family and in the same area underscores our lack of knowledge for several groups and areas of the tropics. It is important to emphasize that every one of the three species described here has characters that are unique within their respective lineages (see discussions below), thus the discovery of these new species goes beyond that of adding to species to groups and areas, but also greatly add to our knowledge of morphological diversity and evolution for each of the three genera. Moreover, some of the groups described in the last 10 years represent key lineages heretofore unknown. An example is Physeterostemon (Goldenberg & Amorim, 2006), first described from two species from southern Bahia, and that turned out to represent the sister group of the Miconieae (Amorim, Goldenberg & Michelangeli, 2009), an exclusively Neotropical group with ca. 2,000 species.

The description of the species here is as a good example of a Linnean shortfall, because three new species from a single family are found in the same place, disclosing the absence of basic knowledge regarding the biodiversity of the area. As for conservation purposes, the description of these probably endemic species per se is a signal that this area deserves more attention regarding research and policies, but its consequences go farther: this area has a relevant role as a phylogenetic (both genetic and morphological) stock (Vane-Wright, Humphries & Williams, 1991; Faith, 1992; Nee & May, 1997; Sechrest et al., 2002; Hidasi-Neto, Loyola & Cianciaruso, 2013), and thus is also valuable as a phylogenetic conservation priority.

Study Area

The “Estação Ecológica Estadual de Wenceslau Guimarães” (EEEWG) was created in 1997 and enlarged in 2000, totaling 2,418 hectares (Bahia, 2010). The reserve is contained within a single municipality, Wenceslau Guimarães, in the southern portion of the state of Bahia, Brazil (Fig. 1). Its geomorphology includes deep and straight valleys 200–500 m wide, at 550 m elevation at the lowest point, and enclosed by mountains up to 1,000 m elevation, with slopes ranging mostly between 15° and 50°. The soils are mostly alic Oxisols, but there are also Lithic Psamments and Ultisols. The climate is tropical and humid, but some slopes facing west can be considered as sub-humid. The annual mean temperature ranges between 22° and 25.5 °C, and rainfall between 800 and 1,500 mm (Bahia, 2010).

The area surrounding the reserve has been almost entirely logged and cleared. It is nowadays covered with small rural properties, and the agricultural activities are based mostly on cocoa, fruticulture (mostly soursop, locally called “graviola,” and sold as frozen pulp) and subsistence crops. Some areas inside the reserve has been cleared and used for agricultural purposes for a long time up to the 1990s, but now there are no families living in it anymore. Apart from some areas covered with secondary vegetation, mostly on the bottom of the valleys and lower slopes, the reserve is covered with sub-montane tropical moist forest (“Floresta Ombrófila Densa Submontana,” according to the Brazilian official classification system; Veloso, Rangel-Filho & Lima, 1991). On slopes up to 50°, the canopy is 8–15 m high, and average trunk diameter 15–30 cm, with remnant trees up to 30 m tall and 1 m diameter; the understory is well developed and the trees usually heavy with epiphytes. The vegetation on slopes above 800 m is lower, the canopy at 3–6 m, and average trunk diameter 5–10 cm, with a dense moss and lichen cover. Steeper and more exposed slopes and some mountain tops are covered with sparse vegetation, with a mosaic of shrubs and herbs on lithic soils.

Figure 1: Map with the collection localities in the municipality of Wenceslau Guimarães, Bahia, Brazil.

Botanical exploration in the area is recent. They began in the early 1990s, with A.M. Carvalho, F. França, E. Melo, S. Mayo, W.W. Thomas and S.C. Sant’Anna. Surprisingly there are only three new species of plants described with types from Wenceslau Guimarães, all of them bromeliads (Leme & Luther, 1998; Leme, 1999; Leme & Luther, 2003). There is also a new species of treefrog (Anura) described for the area (Caramaschi & Rodrigues, 2003).

The electronic version of this article in Portable Document Format (PDF) will represent a published work according to the International Code of Nomenclature for algae, fungi, and plants (ICN), and hence the new names contained in the electronic version are effectively published under that Code from the electronic edition alone. In addition, new names contained in this work which have been issued with identifiers by IPNI will eventually be made available to the Global Names Index. The IPNI LSIDs can be resolved and the associated information viewed through any standard web browser by appending the LSID contained in this publication to the prefix “http://ipni.org/”. The online version of this work is archived and available from the following digital repositories: PeerJ, PubMed Central, and CLOCKSS.

Diagnosis. A species of Huberia that differs from all other species in the genus due to the sessile leaves with subcordate to cordate bases, short (1–1.3 mm long) sepals, and the connective with a very short (1.3–1.7 mm long) dorsal tooth.

Description. Trees or shrubs 4–5 m high, with few erect branches. Young stems, leaves, inflorescences and hypanthia glutinose (both in fresh and dry specimens), covered with glandular trichomes with very short stalks, which are more distinctive on both leaf surfaces, where they are located on depressions and look more like dots than trichomes, otherwise glabrous. Young stems slightly quadrangular or slightly 4-sulcate, later becoming terete; interpetiolar lines absent. Leaves opposite, isomorphic, bigger on the proximal portions of the branches, then gradually smaller towards the apex; petioles absent when seen in adaxial view, but the leaves have a thick, rounded, 1–1.5 mm long protuberance at the base, in abaxial view, that may be interpreted as a reduced petiole; blades on fertile branches (2-)3–5 × (1-)1.7–3.7 cm, chartaceous, ovate to ovate-elliptic, base subcordate to cordate, apex broadly acute to obtuse or rounded, margin entire and narrowly hyaline; blades on sterile branches larger than on the fertile branches, up to 9 × 5 cm, apex obtuse to acute, margins denticulate; venation acrodromous, basal, lacking domatia, with one pair of secondaries, elevated on abaxial surface, and with an additional pair of faint submarginal veins, tertiary veins percurrent but barely perceptible, quaternaries and areoles not perceptible in both surfaces. Inflorescence usually a single terminal, erect, 7–13-flowered umbellate cyme, 2–2.7 cm long, with a pair of bracts 1.4–2.3 × 0.9–1.3, leafy, sessile, oval to lanceolate, apex rounded, on a peduncle 1.6–2.2 cm long, or the inflorescences with one central and two lateral axes (totaling 20–30 flowers), each one similar to the cyme described above, but the laterals on peduncles 2–3 cm long, lacking bracts; bracteoles 2 per cluster, 2.3–7 × 1–2 mm, sessile, oblong to lanceolate, apex rounded. Flowers 4-merous, on pedicels 5.5–7 mm long. Hypanthium green, 5.5–6.5 × 2–2.5 mm, terete to oblong-urceolate, surface smooth (not alate, nor costate). Calyx opening regularly; tube 0.6–0.9 mm tall; sepals 1–1.3 mm long, broadly deltoid; dorsal teeth 0.5–0.7 mm. long, longitudinally flattened, triangular to rounded (then more prominent and rounded in fruits). Petals white, 11–13 × 8–9.5 mm, asymmetrically obovate, the apex rounded but with a sub-apical tooth, papillose. Stamens 8, isomorphic, all bent to to one side of the flower at anthesis, yellow but turning orange–red in older flowers; filaments 6–7.5 mm long; connective not extended below the thecae but with a dorsal, straight, subulate tooth 1.3–1.7 mm long; thecae 7.7–8.5 mm long, sigmoid, corrugated, opening by a ventrally inclined pore. Ovary 4–4.5 mm long, ca. 1/2 superior, 4-locular; style sigmoid, white or pale-yellow, 13–14.5 mm long, tapering towards the apex, bent to the same side of the flower than the anthers; stigma punctiform. Young capsules (“ruptidio” sensu Baumgratz, 1985), yellowish-green, 10–12 mm long on pedicels 9–11 mm long, urceolate, surface smooth (not alate nor costate), with four longitudinal faint nerves plus four alternating shallow furrows. Mature fruits and seeds not seen.

Distribution and conservation status.Huberia sessilifolia is known from only one population along an exposed rocky ridge within the “Estação Ecológica Estadual Wenceslau Guimarães” in southern Bahia. Given the size of the reserve (24.2 km2) and potential habitat, we recommend that H. sessilifolia is given a status of “critically endangered” (IUCN, 2014).

Etymology. The epithet refers to the sessile leaves, which are the most distinctive feature of this species.

Remarks. All species of Huberia known to date have petiolate leaves, with bases ranging from cuneate and decurrent to obtuse to rounded (Baumgratz, 1997). No described species present the sessile leaves with subcordate to cordate bases found in H. sessilifolia. The character combination of short sepals and short connective appendages can be found in H. glazioviana Cogn. and H. consimilis Baumgratz. However in these species the connective appendage ranges from 1.5 to 4 mm long in the former, and 1.3 to 4.7 mm long in the latter (Baumgratz, 1997), thus usually longer than the 1.3–1.7 mm long ones found in H. sessilifolia. Apart from the petiolate leaves with acute to obtuse bases, H. glazioviana also differ from H. sessilifolia on the pubescent branches and leaves, while H. consimilis differs from H. sessilifolia on the longer (up to 24 mm long) and slenderer pedicels (Baumgratz, 1997).

Distribution and conservation status. Meriania inflata is known from only one collection from forests within the Estação Ecológica Estadual Wenceslau Guimarães in southern Bahia. At the time of collecting the type specimen three individuals were observed. Given the size of the reserve (24.2 km2) and potential habitat, we recommend that Meriania inflata is given a status of “critically endangered” (IUCN, 2014).

Etymology. The epithet refers to the two inflated sacs at the base of the thecae. This character occurs in both Meriania inflata and Meriania tetramera, and makes these two species very distinctive among other species of Meriania.

Remarks. Among the Eastern Brazilian species of Meriania, the indument and anther morphology of M. inflata are very similar to those of M. tetramera (Chiavegatto, 2009; Chiavegatto & Baumgratz, 2008; Chiavegatto & Baumgratz, 2015). This anther morphology with paired sacs at the base of the thecae is not known in any other species in the genus apart from M. inflata and M. tetramera. This feature is undoubtedly associated with the pollination biology of these species, but nothing is known about the natural history of either species. While Meriania tetramera also has greenish petals and plinerved leaves, the two species can be readily distinguished because Meriania tetramera has 4-merous flowers and a calyx closed in bud that opens irregularly. The leaf and hypanthium indument of M. inflata is also similar to that of M. calophylla (Naudin) Triana. However, M. calophylla has narrower leaves that are basally-nerved, much larger flowers with purple to lavender petals at anthesis, and dimorphic stamens with dorsal ascending appendages. In the recent key to Brazilian Meriania (Chiavegatto & Baumgratz, 2015), M. inflata would not fit either of the options in the first couplet as the inflorescences are pendulous or deflexed (as in M. glazioviana Cogn. and M. longipes Triana) but the peduncle is less than 4 cm long (as in all other Brazilian species).

Distribution and Conservation Status. Physeterostemon aonae is known from only one population near the “Estação Ecológica Estadual Wenceslau Guimarães” in southern Bahia. This single population is located outside the reserve in a slope side near a cocoa plantation. Searches for this species in similar habitats within the reserve and other nearby forest patches failed to find another population. Given the restricted size of the known habitat, we recommend that P. aonae is given a status of “critically endangered” (IUCN, 2014).

Remarks. Physeterostemon aonae is similar to P. jardimii, but can be distinguished by the blade rounded to subcordate at the base (vs. acute to narrowly rounded in P. jardimii), hypanthium strigose but not glandulose-setose (vs. strigose and glandular-setose), sepals 1.9–2.1 mm long (vs. 1.2–1.3 mm long), dorsal teeth 4.1–4.3 mm long (vs. 2.9–4.1 mm long) and petals 7.7–8.4 mm long (vs. ca. 7 mm long).

Acknowledgements

We thank the staff from CEPEC for help during fieldwork and general support throughout this study; Bobby Angel for preparing the line drawings; Tiago Mauriz (Rio Tinto) for logistical support; Lucas C. Marinho for the help with the color plates and map; and Walter S. Judd and two anonymous reviewers for the improvements on the original manuscript.

Additional Information and Declarations

Competing Interests

The authors declare there are no competing interests.

Author Contributions

Renato Goldenberg conceived and designed the experiments, performed the experiments, analyzed the data, wrote the paper, reviewed drafts of the paper.

Fabián A. Michelangeli and André M. Amorim conceived and designed the experiments, performed the experiments, analyzed the data, wrote the paper, prepared figures and/or tables, reviewed drafts of the paper.

Funding

RG received a Research Productivity Fellowship from CNPq (306852/2013-6). AMA received a Research Productivity Fellowship from CNPq (306992/2012-4); laboratory work was supported by CNPq (Edital Reflora, 563548/2010-0, Edital PPBIO Mata Atlântica, 457483/2012-1 and Edital Universal, 486079/2013-9). FAM’s field and laboratory work were supported by grants from the NSF (DEB-0818399; DEB-1343612). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

IUCN.2014.Guidelines for Using the IUCN Red List Categories and Criteria. (Version 10.1).Prepared by the Standards and Petitions Subcommittee. Available at http://www.iucnredlist.org/ (accessed 10 December 2015)software

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